Coding principles in fish olfaction as revealed by single unit, EOG and behavioral studies

At present, the principles of coding and codes for individual odorants are not known; however, several coding properties and their limitations emerged. The olfactory code for different odorants must be different to enable olfactory discrimination. We studied elements of the olfactory code that are accessible to combined microelectrode and behavioral techniques. A random sample of spontaneously active olfactory receptor neurons (ORNs) responded to a 15 component mixture of amino acids with suppression, excitation and no change in their activity in the ratio of 6:1:8; ORNs responded to L-arginine (L-Arg) in the ratio of 5:5:60 and to L-cysteine (L-Cys) in the ratio of 10:1:27. ORNs provide information that enables nearly an unlimited behavioral discrimination of single odorants. Underwater electro-olfactogram (EOG) recordings from the olfactory organ measure the odorant-induced summed dc potential change from all the olfactory receptor neurons. In behavioral studies, the more (most) stimulatory component of the binary (ternary) mixture determined in EOG recordings was its better-perceived component; however, discrimination conditioning--repeated presentation of the conditioned mixture and its more stimulatory component alone--enabled the discrimination of the conditioned binary and ternary mixtures from their more (most) stimulatory components. In large multimixtures (13 components), where one amino acid is the more potent EOG stimulus than the other less stimulatory but equipotent components, catfish discriminated all single components from the conditioned multimixture. These results indicate that the multi-mixture is not detected as its most stimulatory component. Catfish also do not learn to discriminate a 13 component multimixture from a 12 component multimixture comprising 12 of the same components. Taken together, these findings indicate that the capacity for parallel transfer of mixture component information is limited in the catfish olfactory system. The finding of a limited capacity of multimixture component detection in catfish also supports the hypothesis of across nerve pattern coding of odorants and eliminates the sole existence of entirely specialized olfactory receptor neurons and labeled lines.